Observations by Dr. James Cook
ARS and Washington State University
March 6, 1997
Dr. James Cook, a member of the National Academy of Sciences and leading expert in root health and soil microbial biocontrol, has provided a fascinating summary of work he and colleagues did on ethylene starting over 20 years ago. We will post excerpts from the articles cited by Dr. Cook in the near future. We would welcome other thoughts, suggestions and references, since there is going to be an effort to design some field experiments this summer, as part of the WWF-WPVGA potato IPM project in Wisconsin and no doubt in some other locations as well in light of these recent findings.
Dr. Cook can be contacted at USDA-ARS Department of Plant Pathology, 367 Johnson Hall, Pullman, Washington 99164. Phone:509-335-3772.
Alan Smith in Sydney Australia and I showed and reported in a paper to Nature that ethylene production in soil could not be from fungi on the basis that 1) fungi are aerobic organisms yet ethylene production from soil is prevented by oxygen and enhanced by replacing soil oxygen with any of the gases nitrogen, helium, argon, or hydrogen, and 2) could be prevented by purging the soil with live steam (100 C) but was not phased by treating the soil with aerated steam at temperatures up to 80 C.
We used some unique equipment that allowed us to precisely treat soils with moist heat at temperatures ranging from 60 to 100 C. Fungi are knocked out at 60 C but only spore forming bacteria survive 80 C, according to extensive prior studies with heat pasteurization of soil. Our work with different soil atmospheres was supported by other work showing that addition of factors such as ferrous and nitrate to lower or poise the redox potential of soil pointed clearly to the need for redox potentials below -200 mv, well below the redox of soil in equilibrium with an oxygen atmosphere. This work is published in Nature 252:703-705 (1974).
We then did a study of the influence of soil water potential on endogenous production of ethylene from soil. We showed that ethylene production was prevented by matric potentials of -1 to -1.5 MPa (= -10 to -15 bars). In some of my earlier work with soil physicist Robert I Papendick, we showed that bacterial activity cuts out at soil matric potentials of -10 to -15 bars, but fungi are active at least down to -30 bars and many fungi are active down to -100 bars. For reference, the equilibrium relative humidity of the pore space in a soil at -15 bars is 99%; at -30 bars, 98%, at -45 bars, 97%, etc. Thus, a fungus that can grown at RH values down to 94% is equivalent to it growing at water potentials down to about -90 bars. If fungi are the main sources of ethylene, it should have been detected well below soil water potentials of -10 to -15 bars.
Of course, we must consider the possibility that a particular metabolic function cuts out at a higher water potential than growth itself. The point is that the pattern in relation to water potential, like our data published in the Nature article, is consistent with our hypothesis that ethylene is produced by bacteria. Our data pointed more specifically to spore forming anaerobic bacteria, which means Clostridium or similar bacteria. These organisms are present in soil at populations of log 4-5 colony forming units per gram, and these organisms are well known to produce organic gases. Our paper on water potential is published in the Canadian J. Microbiology 23:811-817 (1977).
Finally, one of my PhD students, John Sutherland, did his thesis at WSU on the effects of chemical and heat treatments of soil on ethylene production. To make a long story short, he showed that the addition of antibacterial agents such as chloramphenicol and novobiocin to soil inhibited ethylene production whereas the addition of cycloheximide, an inhibitor of eukaryotic organisms, had no effect. You must know that any experiments involving the addition of antibiotics to soil are tricky, and overcoming these limitations so as to obtain data that were interpretable was a major part of John's work. This paper is in Soil Biology and Biochemistry 12:357-362 (1980).
John's thesis was my last involvement with ethylene production from soil. However, I have not stopped thinking about this most interesting soil microbiological process as to its implications for root diseases, soilborne pathogens, and soil and root biology. Ethylene in soil affects plant growth, almost certainly, both positively and negatively, depending on the plant, plant part, and concentration. Ethylene accumulates in water logged soils (anaerobic conditions) and in soils amended with organic material (again, increased oxygen consumption in response to the fresh substrate will coordinately increase the volume of oxygen-free (reduced) microsites in soil where the anaerobes are poised to kick into gear).
Alan Smith published a paper in the very early 1970s suggesting that ethylene in soil accounts for the widespread soil fungistasis (the phenomenon whereby fungal spores do not germinate in soil without a source of nutrients, even though the same fungal spores outside the soil environment germinate in water only). However, this explanation for fungistasis does not seem to have held up to scientific testing.
Based on Alan's hypothesis for a role of ethylene in soil fungistasis, Alan and I hypothesized the aerobe/anaerobe cycle whereby, according to our idea, as aerobes consume the oxygen, thereby increasing the volume of anaerobic microsites, anaerobes become active, and produce ethylene. In response to increasing concentrations of ethylene, aerobes became less active (based on the assumption that the gases act as a fungistat in soil), which slows down the consumption of oxygen and arrests the growth of anaerobes. With less growth of anaerobes, the concentration of ethylene drops and up comes the growth of aerobes. This is a great idea, but the evidence has not been forthcoming to show that ethylene in soil arrests the growth of aerobes.
Chuck: This is the summation of my involvement in and thoughts about ethylene in soil. It deserves much more work, as you obviously recognize. I will send you copies of these three papers.
Dr. James Cook